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Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth

Droplet evaporation is a general process in unsaturated environments that results in micro-scale hydrodynamic flows which in turn determine the spatial distributions of microbial cells across surfaces. These spatial distributions can have significant effects on the development and functioning of sur...

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Autores principales: Ruan, Chujin, Borer, Benedict, Ramoneda, Josep, Wang, Gang, Johnson, David R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10444754/
https://www.ncbi.nlm.nih.gov/pubmed/37608025
http://dx.doi.org/10.1038/s41522-023-00428-x
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author Ruan, Chujin
Borer, Benedict
Ramoneda, Josep
Wang, Gang
Johnson, David R.
author_facet Ruan, Chujin
Borer, Benedict
Ramoneda, Josep
Wang, Gang
Johnson, David R.
author_sort Ruan, Chujin
collection PubMed
description Droplet evaporation is a general process in unsaturated environments that results in micro-scale hydrodynamic flows which in turn determine the spatial distributions of microbial cells across surfaces. These spatial distributions can have significant effects on the development and functioning of surface-associated microbial communities, with consequences for important processes such as the spread of plasmids. Here, we experimentally quantified how evaporation-induced hydrodynamic processes modulate the initial deposition patterns of microbial cells (via the coffee ring effect and Marangoni convection) and how these patterns control the spread of an antibiotic resistance-encoding plasmid during surface-associated growth. We found that plasmid spread is a function of the initial density of cells deposited along the droplet periphery, which is a manifestation of the coffee ring effect. Using an individual-based model, we systematically linked how the different initial cell deposition patterns caused by the relative strengths of the coffee ring effect and Marangoni convection determine the extent of plasmid transfer during surface-associated growth. Our study demonstrates that evaporation-induced hydrodynamic processes that are common in nature can alter crucial ecological properties of surface-associated microbial communities and control the proliferation of plasmids, with consequences on the spread of antibiotic resistance and other plasmid-encoded traits.
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spelling pubmed-104447542023-08-24 Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth Ruan, Chujin Borer, Benedict Ramoneda, Josep Wang, Gang Johnson, David R. NPJ Biofilms Microbiomes Article Droplet evaporation is a general process in unsaturated environments that results in micro-scale hydrodynamic flows which in turn determine the spatial distributions of microbial cells across surfaces. These spatial distributions can have significant effects on the development and functioning of surface-associated microbial communities, with consequences for important processes such as the spread of plasmids. Here, we experimentally quantified how evaporation-induced hydrodynamic processes modulate the initial deposition patterns of microbial cells (via the coffee ring effect and Marangoni convection) and how these patterns control the spread of an antibiotic resistance-encoding plasmid during surface-associated growth. We found that plasmid spread is a function of the initial density of cells deposited along the droplet periphery, which is a manifestation of the coffee ring effect. Using an individual-based model, we systematically linked how the different initial cell deposition patterns caused by the relative strengths of the coffee ring effect and Marangoni convection determine the extent of plasmid transfer during surface-associated growth. Our study demonstrates that evaporation-induced hydrodynamic processes that are common in nature can alter crucial ecological properties of surface-associated microbial communities and control the proliferation of plasmids, with consequences on the spread of antibiotic resistance and other plasmid-encoded traits. Nature Publishing Group UK 2023-08-22 /pmc/articles/PMC10444754/ /pubmed/37608025 http://dx.doi.org/10.1038/s41522-023-00428-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Ruan, Chujin
Borer, Benedict
Ramoneda, Josep
Wang, Gang
Johnson, David R.
Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
title Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
title_full Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
title_fullStr Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
title_full_unstemmed Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
title_short Evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
title_sort evaporation-induced hydrodynamics control plasmid transfer during surface-associated microbial growth
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10444754/
https://www.ncbi.nlm.nih.gov/pubmed/37608025
http://dx.doi.org/10.1038/s41522-023-00428-x
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